Flexible B₁₂ ecophysiology of <i>Phaeocystis antarctica</i> due to a fusion B₁₂-independent methionine synthase with widespread homologues.

Abstract

Coastal Antarctic marine ecosystems are significant in carbon cycling because of their intense seasonal phytoplankton blooms. Southern Ocean algae are primarily limited by light and iron (Fe) and can be co-limited by cobalamin (vitamin B₁₂). Micronutrient limitation controls productivity and shapes the composition of blooms which are typically dominated by either diatoms or the haptophyte <i>Phaeocystis antarctica</i>. However, the vitamin requirements and ecophysiology of the keystone species <i>P. antarctica</i> remain poorly characterized. Using cultures, physiological analysis, and comparative omics, we examined the response of <i>P. antarctica</i> to a matrix of Fe-B₁₂ conditions. We show that <i>P. antarctica</i> is not auxotrophic for B₁₂, as previously suggested, and identify mechanisms underlying its B₁₂ response in cultures of predominantly solitary and colonial cells. A combination of proteomics and proteogenomics reveals a B₁₂-independent methionine synthase fusion protein (MetE-fusion) that is expressed under vitamin limitation and interreplaced with the B₁₂-dependent isoform under replete conditions. Database searches return homologues of the MetE-fusion protein in multiple <i>Phaeocystis</i> species and in a wide range of marine microbes, including other photosynthetic eukaryotes with polymorphic life cycles as well as bacterioplankton. Furthermore, we find MetE-fusion homologues expressed in metaproteomic and metatranscriptomic field samples in polar and more geographically widespread regions. As climate change impacts micronutrient availability in the coastal Southern Ocean, our finding that <i>P. antarctica</i> has a flexible B₁₂ metabolism has implications for its relative fitness compared to B₁₂-auxotrophic diatoms and for the detection of B₁₂-stress in a more diverse set of marine microbes.